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The Systematics of the Worldwide Endoparasite Family Apodanthaceae (Cucurbitales), with a Key, a Map, and Color Photos of Most Species

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The Systematics of the Worldwide Endoparasite Family Apodanthaceae (Cucurbitales), with a Key, a Map, and Color Photos of Most Species A peer-reviewed open-access journal PhytoKeysThe 36: 41–57systematics (2014) of the worldwide endoparasite family Apodanthaceae (Cucurbitales)... 41 doi: 10.3897/phytokeys.36.7385 RESEARCH ARTICLE www.phytokeys.com Launched to accelerate biodiversity research The systematics of the worldwide endoparasite family Apodanthaceae (Cucurbitales), with a key, a map, and color photos of most species Sidonie Bellot1, Susanne S. Renner1 1 Systematic Botany and Mycology, University of Munich (LMU), Menzinger Strasse 67, 80638 Munich, Germany Corresponding author: Sidonie Bellot ([email protected]) Academic editor: H. De Boer | Received 26 February 2014 | Accepted 2 April 2014 | Published 30 April 2014 Citation: Bellot S, Renner SS (2014) The systematics of the worldwide endoparasite family Apodanthaceae (Cucurbitales), with a key, a map, and color photos of most species. PhytoKeys 36: 41–57. doi: 10.3897/phytokeys.36.7385 Abstract Using morphological, nuclear, and mitochondrial data, we here revise the taxonomy of Apodanthaceae and allocate the 36 names published in the family to ten biological species in two genera, Apodanthes and Pilostyles. All species are endo-parasites that live permanently inside trees or shrubs of the families Salicaceae or Fabaceae and that only emerge to flower. Because of this life history, Apodanthaceae are among the least known families of flowering plants. Nevertheless, the World’s herbaria as of 2013 hold at least 785 collections that, in combination with DNA phylogenies, permit well-founded species circum- scriptions and geographic range maps. We also provide a key to all species, discuss the newly accepted or synonymized names, and make available color photos of six of the ten species. Keywords Apodanthaceae, genus circumscriptions, mitochondrial DNA sequences, nuclear DNA sequences, parasitic plants, species circumscriptions Introduction Apodanthaceae Tiegh. ex Takht. (Cucurbitales) is a family of endoparasites that live entirely in their host’s stems and only become visible once the strictly unisexual flowers have burst through the bark. This life style, added to the small size of the flowers and Copyright S. Bellot, S.S. Renner. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 42 Sidonie Bellot & Susanne S. Renner / PhytoKeys 36: 41–57 (2014) patchy occurrence of the apparently mostly dioecious populations, has made it difficult to collect good and complete herbarium material (including both sexes and flowering and fruiting specimens). While populations once identified may be recollected at the same time year after year, usually only local botanists will have the opportunity to carry out such recollections. Apodanthaceae are disjunctly distributed in North and South America, mainland Africa, Iran, and Australia. They occur in arid as well as humid tropical environments. Two genera have been validly described, the worldwide Pilo- styles, and Apodanthes from Central and South America. The taxonomy of the genera and species of Apodanthaceae has not been studied since the work of Ida de Vattimo-Gil (Vattimo-Gil 1950, 1955, 1971, 1973). Modern molecular-phylogenetic work based on representatives of most of the so-far named species (Bellot and Renner in review), together with study of collections deposited in the World’s herbaria since the end of the 19th century, has revealed the need to syn- onymize many superfluous names, a task that we carry out here. We also up-date the circumscription of the family and its two genera, and clarify that they have specialized on different hosts, namely Salicaceae (mainlyCasearia ) and Fabaceae. To achieve a better understanding of species boundaries and relationships, and to clarify the species’ geographic and host ranges, we compared loans from numerous her- baria, dissected flowers, and isolated DNA from multiple collections. Molecular mark- ers useful for these obligatory holoparasites are the nuclear 18S ribosomal RNA region and mitochondrial matR (Barkman et al. 2004; Bellot and Renner in review), and we show here that these markers can be used to place incomplete collections (for example, those of only one sex or only with fruits) in the correct species. Lastly, we provide an annotated key to all species that we recognize, and brief descriptions of their diagnostic traits along with color images and comments on their geographic and host ranges. Methods Plant material, DNA extraction and sequencing, phylogenetic analyses We enlarged the DNA data matrix of Bellot and Renner (in review) by extracting DNA from additional specimens representing either unusual individuals or potential new species. No DNA sequences could be obtained from P. stawiarskii, known only from two collections in R, and P. holtzii, the only collection of which was destroyed in World War II. Suppl. material 1 shows species names and their authors, herbarium vouchers, and GenBank accession numbers. In total, 10 sequences (3 of 18S and 7 of matR) were newly generated for this study. Total genomic DNA was extracted from herbarium specimens using the commer- cial plant DNA extraction Invisorb® Spin Plant Mini Kit (Stratec molecular, Berlin, Germany). The mitochondrialmatR and the nuclear 18S genes were amplified using the primers listed in Bellot and Renner (in review). PCR products were purified with the ExoSAP or FastAP clean-up kits (Fermentas Life Sciences, St. Leon-Rot, Germany), and sequencing relied on the Big Dye Terminator v. 3.1 cycle sequencing kit (Applied The systematics of the worldwide endoparasite family Apodanthaceae (Cucurbitales)... 43 Biosystems, Foster City, CA, USA) and an ABI 3130-4 automated capillary sequencer. Chromatograms were checked and sequences were edited using Geneious R7 (Biomat- ters, available from http://www.geneious.com), and contigs were then blasted against GenBank to rule out contamination. Alignments of the clean sequences were performed using the program MAFFT v. 7 (Katoh 2013) resulting in matrices of 1626 and 1727 aligned nucleotides for matR and 18S, respectively. We failed to amplify the gene matR from the African Pilostyles aethiopica and from the Iranian P. haussknechtii. Phylogenetic reconstructions relied on maximum likelihood (ML) as implemented in RAxML-7.2.8- ALPHA (Stamatakis 2006), using the GTR + G model of nucleotide substitution with 100 bootstrap replicates under the same model. Trees were rooted on Corynocarpus laevigatus (Corynocarpaceae; Cucurbitales), based on Filipowicz and Renner (2010). Morphological data and assessment of the host ranges of Apodanthaceae We geo-referenced locality data from 785 herbarium collections on loan from the her- baria B, G, C, GH, K, M, MO, MSB, W, NA, PMA, and SI and added data from the Global Biodiversity Information Facility (GBIF Backbone Taxonomy, 2013-07- 01, http://www.gbif.org/species/7279680). We also recorded host names, up-dating their taxonomy as relevant. All label information was compiled in a database using the Botanical Research and Herbarium Management System (BRAHMS, http://herbaria. plants.ox.ac.uk/), and maps were produced using DIVA-GIS 7.5 (http://www.diva-gis. org). Collections were sorted by geography, flowering specimens were sexed to evaluate sexual dimorphism, and a representative number of flowers were then dissected under a stereoscope. For each dissected flower, the first author recorded the number, arrange- ment and size of the tepals, shape and ornament of the pistil/central column, number of pollen sacs, presence of hairs and presence of a nectary at the base of the flower. Pictures of representative organs were taken using a Dino-Lite USB microscope model AM413ZT (Dino-Lite Europe) and the DinoCapture Imaging software version 2.0 of the same company. Results and discussion Genus and species boundaries in Apodanthaceae The dissections showed that species have characteristic flower sizes, number of tepals, tepal cilia, and number of anthers rings. For the American species, we use these dif- ferences in the key (below). Suppl. material 2 shows measurements and counts from the 123 dissected flowers. Six collections could not reliably be assigned to these groups because their flowers were slightly unusual: R. Callejas et al. 8062, a male plant from Colombia identified as Apodanthes caseariae by A. Idarraga in 2002; Y. Mexia 4540, a female plant from Brazil that is the type of the name A. minarum; H. S. Irwin et al. 20350, a female plant from Brazil identified asPilostyles ulei by Ida de Vattimo 44 Sidonie Bellot & Susanne S. Renner / PhytoKeys 36: 41–57 (2014) in 1975; H.S. Irwin 31560, a male plant identified as P. blanchetii by the first author but parasitizing an uncommon host (Dioclea, Fabaceae); J. Rzedowski 11303, a female plant from Mexico identified by the collector as P. thurberi; and F. Chiang 9034, a fe- male plant from Mexico identified as P. thurberi by J. Henrickson in 1972. The 18S and matR molecular trees show the Pilostyles collections that we wanted to identify (in red on Fig. 1) grouped with P. thurberi or P. blanchetii. The collections R. Callejas et al. 8062 and Y. Mexia 4540 grouped with two undoubted representa- tives of A. caseariae. R. Callejas et al. 8062 is a male plant and comes from the border with Panama, a country where A. caseariae has been repeatedly collected. The host of R. Callejas et al. 8062 was originally identified asTrema (Cannabaceae), but a partial matR sequence of this host BLASTed to Casearia nitida, making it likely that the host was in fact a Casearia. If that is the case, this would suggest that the collection repre- sents an Apodanthes. The few male flowers of Apodanthes caseariae that have so far been dissected (Suppl. material 2) do not allow assessing the full morphological variability of the male flowers of this species. Therefore we had to rely on DNA for identifica- tion. In terms of its matR (Fig. 1A) R. Callejas et al. 8062 was embedded among other sequences of A.
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